Unveiling the co-phylogeny signal between plunderfish Harpagifer spp. and their gut microbiomes across the Southern Ocean.

Understanding the factors that sculpt fish gut microbiome is challenging, especially in natural populations characterized by high environmental and host genomic complexity. However, closely related hosts are valuable models for deciphering the contribution of host evolutionary history to microbiome assembly, through the underscoring of phylosymbiosis and co-phylogeny patterns. Here, we propose that the recent diversification of several Harpagifer species across the Southern Ocean would allow the detection of robust phylogenetic congruence between the host and its microbiome. We characterized the gut mucosa microbiome of 77 individuals from four field-collected species of the plunderfish Harpagifer (Teleostei, Notothenioidei), distributed across three biogeographic regions of the Southern Ocean. We found that seawater physicochemical properties, host phylogeny, and geography collectively explained 35% of the variation in bacterial community composition in Harpagifer gut mucosa. The core microbiome of Harpagifer spp. gut mucosa was characterized by a low diversity, mostly driven by selective processes, and dominated by a single Aliivibrio Operational Taxonomic Unit (OTU) detected in more than 80% of the individuals. Nearly half of the core microbiome taxa, including Aliivibrio, harbored co-phylogeny signal at microdiversity resolution with host phylogeny, indicating an intimate symbiotic relationship and a shared evolutionary history with Harpagifer. The clear phylosymbiosis and co-phylogeny signals underscore the relevance of the Harpagifer model in understanding the role of fish evolutionary history in shaping the gut microbiome assembly. We propose that the recent diversification of Harpagifer may have led to the diversification of Aliivibrio, exhibiting patterns that mirror the host phylogeny. IMPORTANCE: Although challenging to detect in wild populations, phylogenetic congruence between marine fish and its microbiome is critical, as it highlights intimate associations between hosts and ecologically relevant microbial symbionts. Our study leverages a natural system of closely related fish species in the Southern Ocean to unveil new insights into the contribution of host evolutionary trajectory on gut microbiome assembly, an underappreciated driver of the global marine fish holobiont. Notably, we unveiled striking evidence of co-diversification between Harpagifer and its microbiome, demonstrating both phylosymbiosis of gut bacterial communities and co-phylogeny of some specific bacterial symbionts, mirroring the host diversification patterns. Given Harpagifer's significance as a trophic resource in coastal areas and its vulnerability to climatic and anthropic pressures, understanding the potential evolutionary interdependence between the hosts and its microbiome provides valuable microbial candidates for future monitoring, as they may play a pivotal role in host species acclimatization to a rapidly changing environment.

Geography, phylogeny and host switch drive the coevolution of parasitic Gyrodactylus flatworms and their hosts.

BACKGROUND: Gyrodactylus is a lineage of monogenean flatworm ectoparasites exhibiting many features that make them a suitable model to study the host-parasite coevolutionary dynamics. Previous coevolutionary studies of this lineage mainly relied on low-power datasets (a small number of samples and a single molecular marker) and (now) outdated algorithms. METHODS: To investigate the coevolutionary relationship of gyrodactylids and their fish hosts in high resolution, we used complete mitogenomes (including two newly sequenced Gyrodactylus species), a large number of species in the single-gene dataset, and four different coevolutionary algorithms. RESULTS: The overall coevolutionary fit between the parasites and hosts was consistently significant. Multiple indicators confirmed that gyrodactylids are generally highly host-specific parasites, but several species could parasitize either multiple (more than 5) or phylogenetically distant fish hosts. The molecular dating results indicated that gyrodactylids tend to evolve towards high host specificity. Speciation by host switch was identified as a more important speciation mode than co-speciation. Assuming that the ancestral host belonged to Cypriniformes, we inferred four major host switch events to non-Cypriniformes hosts (mostly Salmoniformes), all of which occurred deep in the evolutionary history. Despite their relative rarity, these events had strong macroevolutionary consequences for gyrodactylid diversity. For example, in our dataset, 57.28% of all studied gyrodactylids parasitized only non-Cypriniformes hosts, which implies that the evolutionary history of more than half of all included lineages could be traced back to these major host switch events. The geographical co-occurrence of fishes and gyrodactylids determined the host use by these gyrodactylids, and geography accounted for most of the phylogenetic signal in host use. CONCLUSIONS: Our findings suggest that the coevolution of Gyrodactylus flatworms and their hosts is largely driven by geography, phylogeny, and host switches.

Protist symbionts of termites: diversity, distribution, and coevolution.

The symbiosis between termites and their hindgut protists is mutually obligate and vertically inherited. It was established by the late Jurassic in the cockroach ancestors of termites as they transitioned to wood feeding. Since then, protist symbionts have been transmitted from host generation to host generation by proctodeal trophallaxis (anal feeding). The protists belong to multiple lineages within the eukaryotic superphylum Metamonada. Most of these lineages have evolved large cells with complex morphology, unlike the non-termite-associated Metamonada. The species richness and taxonomic composition of symbiotic protist communities varies widely across termite lineages, especially within the deep-branching clade Teletisoptera. In general, closely related termites tend to harbour closely related protists, and deep-branching termites tend to harbour deep-branching protists, reflecting their broad-scale co-diversification. A closer view, however, reveals a complex distribution of protist lineages across hosts. Some protist taxa are common, some are rare, some are widespread, and some are restricted to a single host family or genus. Some protist taxa can be found in only a few, distantly related, host species. Thus, the long history of co-diversification in this symbiosis has been complicated by lineage-specific loss of symbionts, transfer of symbionts from one host lineage to another, and by independent diversification of the symbionts relative to their hosts. This review aims to introduce the biology of this important symbiosis and serve as a gateway to the diversity and systematics literature for both termites and protists. A searchable database with all termite-protist occurrence records and taxonomic references is provided as a supplementary file to encourage and facilitate new research in this field.

Symbionts in Hodgkinia-free cicadas and their implications for co-evolution between endosymbionts and host insects.

IMPORTANCE: Obligate symbionts in sap-sucking hemipterans are harbored in either the same or different organs, which provide a unique perspective for uncovering complicated insect-microbe symbiosis. Here, we investigated the distribution of symbionts in adults of 10 Hodgkinia-free cicada species of 2 tribes (Sonatini and Polyneurini) and the co-phylogeny between 65 cicada species and related symbionts (Sulcia and YLSs). We revealed that YLSs commonly colonize the bacteriome sheath besides the fat bodies in these two tribes, which is different with that in most other Hodgkinia-free cicadas. Co-phylogeny analyses between cicadas and symbionts suggest that genetic variation of Sulcia occurred in Sonatini and some other cicada lineages and more independent replacement events in the loss of Hodgkinia/acquisition of YLS in Cicadidae. Our results provide new information on the complex relationships between auchenorrhynchans and related symbionts.

Single-colony sequencing reveals microbe-by-microbiome phylosymbiosis between the cyanobacterium Microcystis and its associated bacteria.

BACKGROUND: Cyanobacteria from the genus Microcystis can form large mucilaginous colonies with attached heterotrophic bacteria-their microbiome. However, the nature of the relationship between Microcystis and its microbiome remains unclear. Is it a long-term, evolutionarily stable association? Which partners benefit? Here we report the genomic diversity of 109 individual Microcystis colonies-including cyanobacteria and associated bacterial genomes-isolated in situ and without culture from Lake Champlain, Canada and Pampulha Reservoir, Brazil. RESULTS: We identified 14 distinct Microcystis genotypes from Canada, of which only two have been previously reported, and four genotypes specific to Brazil. Microcystis genetic diversity was much greater between than within colonies, consistent with colony growth by clonal expansion rather than aggregation of Microcystis cells. We also identified 72 bacterial species in the microbiome. Each Microcystis genotype had a distinct microbiome composition, and more closely related genotypes had more similar microbiomes. This pattern of phylosymbiosis could be explained by co-phylogeny in only two out of the nine most prevalent associated bacterial genera, Roseomonas and Rhodobacter. These phylogenetically associated genera could enrich the metabolic repertoire of Microcystis, for example by encoding the biosynthesis of complementary carotenoid molecules. In contrast, other colony-associated bacteria showed weaker signals of co-phylogeny, but stronger evidence of horizontal gene transfer with Microcystis. These observations suggest that acquired genes are more likely to be retained in both partners (Microcystis and members of its microbiome) when they are loosely associated, whereas one gene copy is sufficient when the association is physically tight and evolutionarily long-lasting. CONCLUSIONS: We have introduced a method for culture-free isolation of single colonies from nature followed by metagenomic sequencing, which could be applied to other types of microbes. Together, our results expand the known genetic diversity of both Microcystis and its microbiome in natural settings, and support their long-term, specific, and potentially beneficial associations. Video Abstract.

When are pathogen dynamics likely to reflect host population genetic structure?

Does the structure and connectivity of host populations influence the dynamics and evolution of their pathogens? This topical question is the essence of research investigating the ecology of a Pteropus fruit bat and its zoonotic Nipah virus (NiV) published by Olival et al. in this issue of Molecular Ecology. Questioned less overtly, but nonetheless implicit to the study, is "what are the mechanisms underpinning intraspecific host-pathogen congruence (IHPC) of genetic structure?". Olival et al. investigated the phylogeographical structure of Pteropus medius and NiV isolates across Bangladesh, from areas inside and outside of the Nipah belt-an area where most human spillover events occur. A high degree of host panmixia was discovered, with some population differentiation east of the Nipah belt. NiV genetic structure was congruent with the host. The authors attributed the panmixia and structuring, respectively, to (a) the highly vagile nature of P. medius, and (b) possible differences between bioregions within and outside the Nipah belt. Other potential explanatory mechanisms were acknowledged, including hybridization and transmission mode. This study makes a valuable contribution to a growing body of literature examining IHPC. This has implications not only for pathogen spillover to humans and domestic animals, but more generally for thinking about the mechanisms that underlie patterns of host and pathogen genetic associations.

Mechanisms and Drivers for the Establishment of Life Cycle Complexity in Myxozoan Parasites.

It is assumed that complex life cycles in cnidarian parasites belonging to the Myxozoa result from incorporation of vertebrates into simple life cycles exploiting aquatic invertebrates. However, nothing is known about the driving forces and implementation of this event, though it fostered massive diversification. We performed a comprehensive search for myxozoans in evolutionary ancient fishes (Chondrichthyes), and more than doubled existing 18S rDNA sequence data, discovering seven independent phylogenetic lineages. We performed cophylogenetic and character mapping methods in the largest monophyletic dataset and demonstrate that host and parasite phylogenies are strongly correlated, and that tectonic changes may explain phylogeographic clustering in recent skates and softnose skates, in the Atlantic. The most basal lineages of myxozoans inhabit the bile of chondrichthyans, an immunologically privileged site and protective niche, easily accessible from the gut via the bile duct. We hypothesize that feed-integration is a likely mechanism of host acquisition, an idea supported by feeding habits of chimaeras and ancient sharks and by multiple entries of different parasite lineages from invertebrates into the new host group. We provide exciting first insights into the early evolutionary history of ancient metazoan parasites in a host group that embodies more evolutionary distinctiveness than most other vertebrates.

An evolutionary framework for host shifts - jumping ships for survival.

Host jumping is a process by which pathogens settle in new host groups. It is a cornerstone in the evolution of pathogens, as it leads to pathogen diversification. It is unsurprising that host jumping is observed in facultative pathogens, as they can reproduce even if they kill their hosts. However, host jumps were thought to be rare in obligate biotrophic pathogens, but molecular phylogenetics has revealed that the opposite is true. Here, I review some concepts and recent findings and present several hypotheses on the matter. In short, pathogens evolve and diversify via host jumps, followed by radiation, specialisation and speciation. Host jumps are facilitated by, for example, effector innovations, stress, compatible pathogens and physiological similarities. Host jumping, subsequent establishment, and speciation takes place rapidly - within centuries and millennia rather than over millions of years. If pathogens are unable to evolve into neutral or mutualistic interactions with their hosts, they will eventually be removed from the host population, despite balancing trade-offs. Thus, generally, plant pathogens only survive in the course of evolution if they jump hosts. This is also reflected by the diversity patterns observed in many genera of plant pathogens, where it leads to a mosaic pattern of host groups over time, in which the original host group becomes increasingly obscure.

Co-divergence and tree topology.

In reconstructing the common evolutionary history of hosts and parasites, the current method of choice is the phylogenetic tree reconciliation. In this model, we are given a host tree H, a parasite tree P, and a function [Formula: see text] mapping the leaves of P to the leaves of H and the goal is to find, under some biologically motivated constraints, a reconciliation, that is a function from the vertices of P to the vertices of H that respects [Formula: see text] and allows the identification of biological events such as co-speciation, duplication and host switch. The maximum co-divergence problem consists in finding the maximum number of co-speciations in a reconciliation. This problem is NP-hard for arbitrary phylogenetic trees and no approximation algorithm is known. In this paper we consider the influence of tree topology on the maximum co-divergence problem. In particular we focus on a particular tree structure, namely caterpillar, and show that-in this case-the heuristics that are mostly used in the literature provide solutions that can be arbitrarily far from the optimal value. Then, we prove that finding the max co-divergence is equivalent to compute the maximum length of a subsequence with certain properties of a given permutation. This equivalence leads to two consequences: (1) it shows that we can compute efficiently in polynomial time the optimal time-feasible reconciliation and (2) it can be used to understand how much the tree topology influences the value of the maximum number of co-speciations.

Phylogeography of Diaphorina citri (Hemiptera: Liviidae) and its primary endosymbiont, 'Candidatus Carsonella ruddii': an evolutionary approach to host-endosymbiont interaction.

BACKGROUND: In insects, little is known about the co-evolution between their primary endosymbionts and hosts at the intraspecific level. This study examined co-diversification between the notorious agricultural pest Diaphorina citri and its primary endosymbionts (P-endosymbiont), 'Candidatus Carsonella ruddii' at the population level. RESULTS: Maximum likelihood, haplotype network, principal components and Bayesian clustering identified three lineages for D. citri and its P-endosymbiont: a Western clade containing individuals from Pakistan, Bhutan (Phuentsholing), Vietnam (Son La), USA, Myanmar and China (Ruili, Yunnan); a Central clade, with accessions originating from Southwest China, Bhutan (Tsirang) and Bangladesh; and an Eastern clade containing individuals from Southeast Asia, and East and South China. A more diverse genetic structure was apparent in the host mitochondrial DNA than their P-endosymbionts; however, the two sets of data were strongly congruent. CONCLUSION: This study provides evidence for the co-diversification of D. citri and its P-endosymbiont during the migration from South Asia to East and Southeast Asia. We also suggest that the P-endosymbiont may facilitate investigations into the genealogy and migration history of the host. The biogeography of D. citri and its P-endosymbiont indicated that D. citri colonized and underwent a secondary dispersal from South Asia to East and Southeast Asia. © 2018 Society of Chemical Industry.

Genetic diversity and evolution of Pneumocystis fungi infecting wild Southeast Asian murid rodents.

Pneumocystis organisms are airborne-transmitted fungal parasites that infect the lungs of numerous mammalian species with strong host specificity. In this study, we investigated the genetic diversity and host specificity of Pneumocystis organisms infecting Southeast Asian murid rodents through PCR amplification of two mitochondrial genes and tested the co-phylogeny hypothesis among these fungi and their rodent hosts. Pneumocystis DNA was detected in 215 of 445 wild rodents belonging to 18 Southeast Asian murid species. Three of the Pneumocystis lineages retrieved in our phylogenetic trees correspond to known Pneumocystis species, but some of the remaining lineages may correspond to new undescribed species. Most of these Pneumocystis species infect several rodent species or genera and some sequence types are shared among several host species and genera. These results indicated a weaker host specificity of Pneumocystis species infecting rodents than previously thought. Our co-phylogenetic analyses revealed a complex evolutionary history among Pneumocystis and their rodent hosts. Even if a significant global signal of co-speciation has been detected, co-speciation alone is not sufficient to explain the observed co-phylogenetic pattern and several host switches are inferred. These findings conflict with the traditional view of a prolonged process of co-evolution and co-speciation of Pneumocystis and their hosts.

Cophylogenetics and biogeography reveal a coevolved relationship between sloths and their symbiont algae.

Specialized species, like arboreal folivores, often develop beneficial relationships with symbionts to exploit ecologically constrained lifestyles. Although coevolution can drive speciation by specialization of a symbiont to a host, a symbiotic relationship is not indicative of coevolution between host and symbiont. We tested for coevolved relationships between highly specialized two- and three-toed sloths (Choloepus spp. and Bradypus spp., respectively) and their symbiotic algae using cophylogenies and phylogeography. Our phylogeographic analysis showed a biogeographic pattern for the sloth distribution that was not found in the algal phylogeny. We found support for congruence between the sloth and algae phylogenies, implying cospeciation, only in the Bradypus lineage. Algae host-switching occurred from Bradypus spp. to Choloepus spp. Our results support a previously hypothesized symbiotic relationship between sloths and the algae in their fur and indicate that coevolution may have played a role in algae diversification. More broadly, convergent evolution may facilitate host switching between deeply diverged host lineages.

Malagasy bats shelter a considerable genetic diversity of pathogenic Leptospira suggesting notable host-specificity patterns.

Pathogenic Leptospira are the causative agents of leptospirosis, a disease of global concern with major impact in tropical regions. Despite the importance of this zoonosis for human health, the evolutionary and ecological drivers shaping bacterial communities in host reservoirs remain poorly investigated. Here, we describe Leptospira communities hosted by Malagasy bats, composed of mostly endemic species, in order to characterize host-pathogen associations and investigate their evolutionary histories. We screened 947 individual bats (representing 31 species, 18 genera and seven families) for Leptospira infection and subsequently genotyped positive samples using three different bacterial loci. Molecular identification showed that these Leptospira are notably diverse and include several distinct lineages mostly belonging to Leptospira borgpetersenii and L. kirschneri. The exploration of the most probable host-pathogen evolutionary scenarios suggests that bacterial genetic diversity results from a combination of events related to the ecology and the evolutionary history of their hosts. Importantly, based on the data set presented herein, the notable host-specificity we have uncovered, together with a lack of geographical structuration of bacterial genetic diversity, indicates that the Leptospira community at a given site depends on the co-occurring bat species assemblage. The implications of such tight host-specificity on the epidemiology of leptospirosis are discussed.